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Methicillin-resistant Staphylococcus aureus, Hawaii, 2000-2002.



The emergence of methicillin-resistant Staphylococcus aureus methicillin-resistant Staphylococcus aureus Methicillin-aminoglycoside resistant Staphylococcus aureus, MRSA An organism with multiple antibiotic resistances–eg, aminoglycosides, chloramphenicol, clindamycin, erythromycin, rifampin, tetracycline,  (MRSA MRSA Methicillin-resistant Staphylococcus aureus. See MARSA. ) has generated considerable concern among medical and public health professionals. We used a statewide, population-based antimicrobial antimicrobial /an·ti·mi·cro·bi·al/ (-mi-kro´be-al)
1. killing microorganisms or suppressing their multiplication or growth.

2. an agent with such effects.
 resistance surveillance system to examine epidemiologic trends for MRSA from outpatients and inpatients in Hawaii. Pediatric pediatric /pe·di·at·ric/ (pe?de-at´rik) pertaining to the health of children.

pe·di·at·ric
adj.
Of or relating to pediatrics.
 and adult patient populations were compared to assess characteristics of MRSA isolates specific for each group. From 2000 to 2002, 8,206 (26%) of 31,482 total S. aureus The aureus (pl. aurei) was a gold coin of ancient Rome valued at 25 silver denarii. The aureus was regularly issued from the 1st century BC to the beginning of the 4th century AD, when it was replaced by the solidus.  isolates were MRSA. During this period, the proportion of MRSA isolates increased in both outpatient and inpatient clinical settings (p<0.01). When stratified stratified /strat·i·fied/ (strat´i-fid) formed or arranged in layers.

strat·i·fied
adj.
Arranged in the form of layers or strata.
 by age, annual trends showed a significant increase in the proportion of MRSA in adult patients (from 24% to 30%, p<0.01) but not in pediatric patients (from 25% to 27%, p>0.05). Although MRSA isolates from adults demonstrated high resistance to most non-[beta]-lactams, most MRSA isolates from pediatric outpatients remained susceptible to most non-[beta]-lactams.

**********

First detected in the 1960s, methicillin-resistant Staphylococcus aureus (MRSA) has become the leading cause of nosocomial infections Nosocomial infections
Infections that were not present before the patient came to a hospital, but were acquired by a patient while in the hospital.

Mentioned in: Enterobacterial Infections, Staphylococcal Infections
 during the last 2 decades (1). MRSA isolates are increasingly resistant to multiple non-[beta]-lactam antimicrobial drugs. Recent reports of vancomycin-resistant S. aureus foreshadow fore·shad·ow  
tr.v. fore·shad·owed, fore·shad·ow·ing, fore·shad·ows
To present an indication or a suggestion of beforehand; presage.



fore·shad
 an era of chemotherapy in which effective bactericidal bactericidal /bac·te·ri·ci·dal/ (bak-ter?i-si´d'l) destructive to bacteria.
Bactericidal
An agent that destroys bacteria (e.g.
 drugs to treat infection with this organism may not be readily available (2,3).

Established risk factors for MRSA infection include a history of recent hospitalization or surgery, dialysis, residing in long-term care facilities long-term care facility
n.
See skilled nursing facility.
, presence of an indwelling catheter indwelling catheter Any catheter, usually understood to be for the urinary bladder–eg, a 'Foley' left in place for a prolonged period of time , and use of injectable in·ject·a·ble
adj.
Capable of being injected. Used of a drug.

n.
A drug or medicine that can be injected.
 drugs (4-6). More recently, however, outbreaks of MRSA infections have been reported in healthy persons without these previously recognized risk factors in a variety of community settings (7-12).

Preliminary work suggests that community isolates of MRSA differ from their hospital counterparts in their demographic, clinical, and molecular characteristics (13-18). However, the epidemiology of MRSA in outpatient settings has not been fully described. In particular, knowledge is limited regarding the epidemiology of MRSA in persons visiting hospital outpatient settings, public or community health centers, and private physicians' offices, i.e., settings where most MRSA infections are treated and the greatest percentage of total antimicrobial use occurs (19). The objective of this study was to better characterize the epidemiology of MRSA from both inpatient and outpatient settings in Hawaii by using a population-based surveillance system.

Materials and Methods

Data Collection

Antimicrobial susceptibility test susceptibility test Antimicrobial susceptibility test, see there  data, collected retrospectively through the State of Hawaii Antimicrobial Resistance Project (SHARP) from 2000 to 2002, were used for this analysis. The SHARP system captures electronic laboratory data from 2 large private clinical laboratories, which serve most of Hawaii's total population (N = 1,211,537) (20). These 2 commercial laboratories provide susceptibility testing services for >85% of all nonhospital outpatient settings in Hawaii (21). They also perform susceptibility testing for 18 of 24 acute care hospitals in the state, including the outpatient services outpatient services Hospital-based services Managed care Medical and other services provided, to a nonadmitted Pt, by a hospital or other qualified facility–eg, mental health clinic, rural health clinic, mobile X-ray unit, free-standing dialysis unit Examples  associated with these hospital facilities (22). The remaining 6 acute care hospitals perform susceptibility testing in their own laboratories. Data from 2 of these hospitals are incorporated into the SHARP database, which provides a final dataset that encompasses 20 (83%) of Hawaii's 24 acute care hospitals.

Isolate-level data, including the specimen collection date, source (e.g., blood, urine, and cerebrospinal fluid cerebrospinal fluid (CSF)

Clear, colourless liquid that surrounds the brain and spinal cord and fills the spaces in them. It helps support the brain, acts as a lubricant, maintains pressure in the skull, and cushions shocks.
), susceptibility testing methods (e.g., Kirby-Bauer), and susceptibility test results, are provided by the laboratories participating in SHARP. Limited demographic patient information is also included in the record, e.g., date of birth and sex. However, detailed clinical histories and patient names are not available. In lieu of names, patients were assigned personal identifiers created by concatenating values from the birth date, sex, reporting laboratory, and hospital/clinic location of specimen collection.

All cultures that yielded S. aureus isolates from 2000 through 2002 were identified, and any isolates from patients in nonacute care beds (i.e., long-term care long-term care (LTC),
n the provision of medical, social, and personal care services on a recurring or continuing basis to persons with chronic physical or mental disorders.
 homes) and correctional facilities were excluded. Duplicate isolates were then removed according to according to
prep.
1. As stated or indicated by; on the authority of: according to historians.

2. In keeping with: according to instructions.

3.
 Clinical and Laboratory Standards Institute (formerly NCCLS NCCLS National Committee for Clinical Laboratory Standards ) guidelines (23). Only the first isolate per patient, irrespective of irrespective of
prep.
Without consideration of; regardless of.

irrespective of
preposition despite 
 body site, antimicrobial susceptibility profile, or other phenotypic characteristics (e.g., biotype biotype /bio·type/ (bi´o-tip)
1. a group of individuals having the same genotype.

2. any of a number of strains of a species of microorganisms having differentiable physiologic characteristics.
), in a defined period (for our purposes, 90 days) was included. Therefore, after the initial isolate, successive isolates for the same patient during the next 90 days were excluded.

The breakpoint The location in a program used to temporarily halt the program for testing and debugging. Lines of code in a source program are marked for breakpoints. When those instructions are about to be executed, the program stops, allowing the programmer to examine the status of the program  for MRSA was an MIC [greater than or equal to] 4 [micro]g/mL or a zone diameter [less than or equal to] 10 mm. The breakpoint for oxacillin oxacillin /ox·a·cil·lin/ (ok?sah-sil´in) a semisynthetic penicillinase-resistant penicillin used as the sodium salt in infections due to penicillin-resistant, gram-positive organisms.  (methicillin methicillin /meth·i·cil·lin/ (meth?i-sil´in) a semisynthetic penicillin highly resistant to inactivation by penicillinase; used as the sodium salt.

meth·i·cil·lin
n.
) intermediate isolates was an MIC 2-4 [micro]g/mL or a zone diameter from 11 to 12 mm. The breakpoint for oxacillin (methicillin)-susceptible isolates was an MIC [less than or equal to] 2 [micro]g/mL or a zone diameter [greater than or equal to] 13 mm. Susceptibility interpretations for other antimicrobial drugs were based also on breakpoints established by NCCLS (24).

Patient Classification

Patients [less than or equal to] 18 years of age were defined as pediatric patients and those [greater than or equal to] 19 years of age as adult patients. Classification of inpatient or outpatient status was based on patients' location at the time of specimen collection. Inpatient isolates were defined as those collected from patients in both regular hospital wards and intensive care units. Outpatient isolates were defined as those collected from patients in 1) an outpatient department, emergency department, ambulatory clinic, or same-day-surgery clinic associated with a hospital, or 2) a private physician's office, community public health center, or university health center.

Data Analysis

The proportion of MRSA was calculated as the number of MRSA isolates divided by the total number of S. aureus isolates during a defined period (e.g., per year) for a given setting (e.g., inpatient) and population (e.g., pediatric). The proportion of MRSA isolates resistant to a specific antimicrobial agent was calculated as the proportion of resistant isolates divided by the total MRSA isolates tested against the particular antimicrobial agent of interest during a defined period. Categorical data categorical data

data relating to category such as qualitative data, e.g. dog, cat, female. It may be nominal when a name is used, e.g. location, breed, or ordinal when a range of categories is used, e.g. calf, yearling, cow.
 analysis was performed using EpiInfo version 6.04c statistical software (Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. , Atlanta, GA, USA). Chi-square and Fisher exact tests were used to compare proportions, and significance was defined as p<0.05. The Kruskal-Wallis test was used to compare median age of patients, and Pearson correlation coefficient Correlation Coefficient

A measure that determines the degree to which two variable's movements are associated.

The correlation coefficient is calculated as:
 was used to determine the correlation of age and MRSA proportions in different clinical settings.

Results

A total of 41,250 S. aureus isolates were identified from combined inpatient and outpatient settings from 2000 to 2002. After removal of duplicate data, 31,482 isolates remained in the analysis; 23,550 were from outpatients, and 7,932 were from hospital inpatients. A total of 8,206 (26%) of all isolates included in the analyses were MRSA. The overall proportion of MRSA from 2000 to 2002 in outpatients was 22% (5,135/23,550) versus 39% (3,071/7,932) for inpatients (p<0.01). Although the proportion of MRSA remained significantly higher in inpatients compared with outpatients each year of the study, an overall significant increase in the proportion of MRSA infections was observed in both clinical settings during the 3-year study period (p<0.01, Table 1). The proportion of MRSA isolates during the 3-year period was significantly higher in pediatric outpatients (24%, 1,092/4,571) than that in adult outpatients (21%, 4,043/18,979; p<0.01). However, adult inpatients had a significantly higher proportion of MRSA isolates (40%, 2,868/7,217) when compared with pediatric inpatients (28%, 203/715; p<0.01).

A significant increase in the proportion of MRSA isolates was observed in all adult patients (from 24% to 30%, p<0.01) during the 3-year study period, and an increasing, although not statistically significant, trend was observed in pediatric patients (Figure 1). When the total MRSA isolates for all study years were examined by 10-year age groups, the proportion of MRSA isolates increased with age in inpatients, but not in outpatients (Figure 2). Correspondingly, inpatients with MRSA infections were significantly older (median age 67 years) than outpatients with MRSA infections (median age 44 years; p<0.01).

[FIGURES 1-2 OMITTED]

Of the 31,482 S. aureus isolates in the analysis, 31,240 (99%) had identifiable specimen sources. Table 2 summarizes the frequency of MRSA anatomic specimen sources for pediatric and adult patients in outpatient and inpatient settings. Wounds were the most common specimen sources for MRSA isolates in both pediatric and adult populations in all clinical settings.

For both adult and pediatric patients, MRSA resistance to non-[beta]-lactam antimicrobial agents Antimicrobial agents

Chemical compounds biosynthetically or synthetically produced which either destroy or usefully suppress the growth or metabolism of a variety of microscopic or submicroscopic forms of life.
 was significantly higher in inpatient isolates than in outpatient isolates for nearly all of the antimicrobial agents tested (p<0.01, Table 3). For all years combined, a significantly higher level of resistance to non-[beta]-lactam antimicrobials was observed in all adult MRSA isolates compared with all pediatric MRSA isolates (p<0.01). Most MRSA isolates from pediatric outpatients remained susceptible to most non-[beta]-lactams, with the exception of erythromycin erythromycin (ĭrĭth'rōmī`sĭn), any of several related antibiotic drugs produced by bacteria of the genus Streptomyces (see antibiotic). , to which 24% of the isolates were resistant.

Discussion

Our analyses identified an increase in the proportion of MRSA for both outpatient and inpatient settings in Hawaii from 2000 through 2002. In the final year of the study, the proportion of MRSA isolates in outpatients and inpatients was notable, i.e., 25% and 42%, respectively.

Whereas high rates of MRSA in inpatient settings have been described previously (1,14), our data highlight an issue of more recent concern, i.e., increasing MRSA infections occurring in the outpatient setting. In the absence of detailed clinical histories, isolates obtained in the outpatient setting cannot be equated to community-associated MRSA. However, isolates from a large population of pediatric outpatients may be a reasonable surrogate for community-associated S. aureus infections because they should reflect infections occurring in a predominantly healthy, nonhospitalized population. Furthermore, previous studies have established that skin and soft tissue infections are the most common sources of community-associated MRSA (16,25,26). In our setting, [approximately equal to] 25% of all S. aureus infections from pediatric outpatients were MRSA, with 95% of these isolated from wounds. These data suggest that MRSA is an important cause of wound infections in children in Hawaii, a finding consistent with a growing number of reports of MRSA in pediatric outpatients elsewhere (27,28).

Although the proportion of MRSA isolates was significantly lower for adult outpatients compared with pediatric outpatients (21% versus 24%, p<0.01), the total number of MRSA infections in adult outpatients outnumbered those in pediatric outpatients nearly 4:1. In addition, we observed a positive correlation Noun 1. positive correlation - a correlation in which large values of one variable are associated with large values of the other and small with small; the correlation coefficient is between 0 and +1
direct correlation
 between the proportion of MRSA isolates and advancing age for inpatients, but not for outpatients (R = 0.92, p<0.01). This finding is not unexpected if one considers that older adults are more likely to have chronic illnesses that require more frequent hospitalizations and, thus, potentially encounter increased exposure to resistant microorganisms (1,4,5,14).

MRSA isolates obtained from outpatient settings tended to be less resistant to nonoxacillin antimicrobial drugs than their inpatient counterparts, as observed elsewhere (12,14,16,25 28). Proportionally more pediatric isolates remained susceptible to multiple non-[beta]-lactams compared with adult isolates, most notably when compared with adult inpatient isolates. The dissimilar antimicrobial resistance profiles observed between clinical settings may reflect differences in cohorts of circulating MRSA isolates, especially between outpatients and inpatients, as has been demonstrated in other investigations (16,27,28).

Of clinical importance is that pediatric outpatient MRSA isolates remained largely susceptible to most non-[beta]-lactams. However, [approximately equal to] 25% of pediatric outpatient MRSA isolates in Hawaii were resistant to erythromycin, which is consistent with findings in other studies of MRSA macrolide resistance in pediatric outpatients (25,27,28). In contrast, only 7% of the pediatric outpatient isolates were resistant to clindamycin. This antimicrobial drug has been used to successfully treat MRSA infections in children in community settings. However, clinicians should be aware of inducible resistance to clindamycin due to methylation methylation,
n a phase-II detoxification pathway in the liver; methyl groups combine with toxins to rid the body of various substances.

methylation
(meth´
 of ribosomal RNA ribosomal RNA
n.
See rRNA.


ribosomal RNA (rī´bōsō´m
 encoded by the genes ermA or ermC in initially clindamycin-susceptible but erythromycin-resistant S. aureus isolates (25,29). Therefore, clindamycin monotherapy should be avoided in critically ill children with MRSA infections until inducible clindamycin resistance has been excluded by double-disk testing (25,29,30).

A major limitation of this study is the potential misclassification of the clinical setting (i.e., outpatient versus inpatient). Because of the lack of named personal identifiers, patients could not be traced from isolates to be interviewed, and medical records could not be reviewed. Therefore, we could not directly correlate our findings for outpatients and inpatients with the more conventional definitions of community-associated and nosocomial-associated MRSA, respectively. We assigned an isolate to a clinical setting based on the location where the patient's specimen was collected, so misclassification was possible. For example, a patient whose specimen was obtained in an outpatient setting (e.g., an emergency department) may have actually acquired S. aureus during a recent hospitalization. If misclassification of this type occurred, the difference in MRSA rates between outpatient and inpatient isolates would be underestimated. However, this misclassification type might be expected to remain consistent over a 3-year period, so the observed temporal trends would likely remain valid. Moreover, the significant differences in resistance to nonoxacillin antimicrobial drugs observed between outpatients and inpatients suggest that the MRSA isolates from outpatients were not, on average, nosocomial-associated isolates cultured in the outpatient setting (13,14,16).

Another study limitation is the inability to fully assess the effect of potential changes in clinical practice during the 3-year study period. If physicians increased or decreased the tendency to obtain cultures, these changes might affect the number or proportion of MRSA isolates identified each year. However, retrospective examination of the total number of cultures requested by physicians each year from 6 acute care hospitals demonstrated that 102,537, 99,772, and 99,461 total cultures were ordered at these facilities in 2000, 2001, and 2002, respectively. These data do not suggest any major shift in practice patterns during the relatively short duration of this study. Therefore, the observed temporal trends cannot likely be attributed to changing physician practices.

A third possible limitation is that we were unable to include susceptibility testing data from 4 of Hawaii's 24 acute care medical centers and their associated outpatient locations. However, a separate review of antibiogram data available from all laboratory facilities in the state in 2001 found that in aggregate, the 4 excluded hospital laboratories accounted for only 1,632 (11%) of the 14,539 total S. aureus isolates identified that year. Therefore, the SHARP data in this study captured [approximately equal to] 90% of all S. aureus susceptibility testing data in Hawaii from 2000 to 2002.

To our knowledge, this is the first study of MRSA using susceptibility testing data from inpatient and outpatient settings representative of an entire state population. Our major finding, substantive and increasing rates of MRSA in the outpatient setting, is particularly important as reports of MRSA acquired in the community increase across the country, and optimal strategies for the management of MRSA infections in the outpatient setting have yet to be established (14,16,25,27-30). More studies are needed to improve the understanding of MRSA epidemiology in the community and to identify appropriate strategies to prevent S. aureus infections, including MRSA.
Table 1. Distribution of methicillin-resistant Staphylococcus aureus
(MRSA) isolates by patient group and clinical setting in Hawaii

                            Outpatients

                                               Contributing
                       No. S.     No. (%)        to total
Year   Patient group   aureus       MRSA         MRSA (%)

2000       Total       7,633    1,557 (20) *        --
         Pediatric     1,593      384 (24)          25
           Adult       6,040     1,173 (19)         75
2001       Total       7,543    1,495 (20) *        --
         Pediatric     1,401      302 (22)          20
           Adult       6,142     1,193 (19)         80
2002       Total       8,374    2,083 (25) *        --
         Pediatric     1,577      406 (26)          19
           Adult       6,797     1,677 (25)         81

                             Inpatients

                                               Contributing
                       No. S.     No. (%)        to total
Year   Patient group   aureus       MRSA         MRSA (%)

2000       Total       2,330     842 (36) *         --
         Pediatric      216       65 (30)           8
           Adult       2,114      777 (37)          92
2001       Total       2,661     997 (37) *         --
         Pediatric      249       53 (21)           5
           Adult       2,412      944 (39)          95
2002       Total       2,941    1,232 (42) *        --
         Pediatric      250       85 (34)           7
           Adult       2,691     1,147 (43)         93

* p<0.001, by chi-square test for trend for outpatient and
inpatient settings.

Table 2. Specimen sources of methicillin-resistant Staphylococcus
aureus isolates from pediatric and adult patients by clinical
setting, Hawaii, 2000-2002

                    Pediatric        Pediatric
                   outpatients     inpatients (%)
Specimen sources   (%) n = 1,086      n = 199

Wound                  95              72
Sputum                  0               1
Urine                   2               2
Blood                   0               4
Other ([dagger])        3              21

                        Adult             Adult
                   outpatients (%)   inpatients (%) *
Specimen sources      n = 4,012         n = 2,829

Wound                    80                 46
Sputum                    4                 29
Urine                     7                  8
Blood                     4                  7
Other ([dagger])          5                  9

* Total percentage may not equal 100% because of rounding.

([dagger]) Includes medical devices, respiratory swabs, gynecologic
specimens, stool, synovial fluid, and gallbladder specimens.

Table 3. Resistance patterns of MRSA isolates from pediatric and
adult patients by clinical setting, Hawaii, 2000-2002 *

                               Pediatric patients

                        Outpatients            Inpatients

                     No.                    No.
Antimicrobial      isolates    No. (%)    isolates    No. (%)
drug               tested *   resistant   tested *   resistant

Ciprofloxacin        604       11 (2)       110       10 (9)
Clindamycin         1,083      71 (7)       202       39 (19)
Erythromycin        1,092     261 (24)      203       78 (38)
Gentamicin           997        9 (1)       199       12 (6)
Levofloxacin         215        5 (2)        59       9 (16)
Rifampin            1,028       4 (0)       199        5 (3)
Tetracycline         812       27 (3)       178       16 (9)
Trimethoprim/       1,092       1 (0)       203        2 (1)
sulfamethoxazole
Vancomycin          1,092       0 (0)       203        0 (0)

                   Pediatric
                   patients         Adult patients

                                      Outpatients

                       p          No.
Antimicrobial        value      isolates    No. (%)
drug               ([dagger])   tested *   resistant

Ciprofloxacin        <0.01       1,502      545 (36)
Clindamycin          <0.01       3,936     1,462 (37)
Erythromycin         <0.01       4,018     2,186 (54)
Gentamicin           <0.01       3,289      418 (13)
Levofloxacin         <0.01        629       245 (39)
Rifampin             <0.01       3,773      134 (4)
Tetracycline         <0.01       3,414      667 (20)
Trimethoprim/          NS        4,035      199 (5)
sulfamethoxazole
Vancomycin             NA        4,036       0 (0)

                              Adult patients

                         Inpatients

                     No.                       p
Antimicrobial      isolates    No. (%)       value
drug               tested *   resistant    ([dagger])

Ciprofloxacin       1,305     1,071 (85)     <0.01
Clindamycin         2,830     2,128 (75)     <0.01
Erythromycin        2,859     2,412 (84)     <0.01
Gentamicin          2,609      906 (35)      <0.01
Levofloxacin         549       433 (79)      <0.01
Rifampin            2,795      355 (13)      <0.01
Tetracycline        2,622      976 (37)      <0.01
Trimethoprim/       2,862      278 (10)      <0.01
sulfamethoxazole
Vancomycin          2,865       0 (0)          NA

* The number of MRSA isolates tested against each antimicrobial drug
varies in each laboratory because the drug panel used differed for
each MRSA. MRSA, methicillin-resistant Staphylococcus aureus; NS,
not significant; NA, not applicable.

([dagger]) By chi-square test comparing outpatients to inpatients
within each patient group. Fisher exact test was used for rifampin
within the pediatric population.


Acknowledgments

We thank all the participating laboratories and hospitals, including the Diagnostic Laboratory Services, Inc., Hawaii, Clinical Laboratories of Hawaii, Kaiser Permanente Kaiser Permanente is an integrated managed care organization, based in Oakland, California, founded in 1945 by industrialist Henry J. Kaiser and physician Sidney R. Garfield. , Straub Clinic and Hospital, and Triplet triplet /trip·let/ (trip´let)
1. one of three offspring produced at one birth.

2. a combination of three objects or entities acting together, as three lenses or three nucleotides.

3.
 Army Medical Center.

This study was supported by the Centers for Disease Control and Prevention Epidemiology and Laboratory Capacity Cooperative Agreement (Grant No.U50/CCU 923810-01).

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(19.) Burt CW, Schappert SM. Ambulatory care ambulatory care
n.
Medical care provided to outpatients.


ambulatory care,
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 DB, Mermel LA. Community-acquired methicillin-resistant Staphylococcus aureus in southern New England New England, name applied to the region comprising six states of the NE United States—Maine, New Hampshire, Vermont, Massachusetts, Rhode Island, and Connecticut. The region is thought to have been so named by Capt.  children. Pediatrics. 2004;113;347-52.

(28.) Buckingham SC, McDougal LK, Cathey LD, Comeaux K, Craig AS, Fridkin SK, et al. Emergency of community-associated methicillin-resistant Staphylococcus aureus at a Memphis, Tennessee For the ancient Egyptian capital, see .

Memphis is a city in the southwest corner of Tennessee, and the county seat of Shelby County. Memphis rises above the Mississippi River on the 4th Chickasaw Bluff just below the mouth of the Wolf River.
 children's hospital A children's hospital is a hospital which offers its services exclusively to children. The number of children's hospitals proliferated in the 20th century, as pediatric medical and surgical specialties separated from internal medicine and adult surgical specialties. . Pediatr Infect Dis J. 2004:23:619-24.

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in vi·tro
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In an artificial environment outside a living organism.
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Fenfang Li, * Sarah Y. Park, ([dagger]) Tracy L. Ayers, ([dagger]) F. DeWolfe Miller, * Ralph MacFadden, ([dagger]) Michele Nakata, ([dagger]) Myra Ching For the Chinese surname Ching 程, see .

For the Chinese dynasty, see .
The ching (Thai: ฉิ่ง; sometimes romanized as chhing) are small bowl-shaped finger cymbals of thick and heavy bronze, with a broad rim commonly used in Cambodia and
 Lee, ([dagger]) and Paul V Paul V, 1552–1621, pope (1605–21), a Roman named Camillo Borghese; successor of Leo XI. He was created cardinal (1596) by Clement VIII and was renowned for his knowledge of canon law. . Effler ([dagger])

* University of Hawaii (body, education) University of Hawaii - A University spread over 10 campuses on 4 islands throughout the state.

http://hawaii.edu/uhinfo.html.

See also Aloha, Aloha Net.
 School of Medicine, Honolulu, Hawaii For the city and county of Honolulu, see City & County of Honolulu.

“Honolulu” redirects here. For other uses, see Honolulu (disambiguation).
Honolulu is the capital as well as the most populous community of the State of Hawaii, United States.
, USA; and ([dagger]) Hawaii Department of Health, Honolulu, Hawaii, USA

Ms. Li is a PhD student at the John A. Burns School of Medicine

The John A. Burns School of Medicine
, University of Hawaii. Her research interests include infectious diseases infectious diseases: see communicable diseases.  epidemiology and development and implementation of active national infectious disease Infectious disease

A pathological condition spread among biological species. Infectious diseases, although varied in their effects, are always associated with viruses, bacteria, fungi, protozoa, multicellular parasites and aberrant proteins known as prions.
 surveillance systems in nonindustrialized countries.

Address for correspondence: Fenfang Li, Disease Outbreak Control Division, Hawaii Department of Health, 1132 Bishop St, Suite 1900, Honolulu, HI 96813, USA; tax: 808-586-4595; email: Fenfang@ hawaii.edu
COPYRIGHT 2005 U.S. National Center for Infectious Diseases
No portion of this article can be reproduced without the express written permission from the copyright holder.
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Title Annotation:RESEARCH
Author:Effler, Paul V.
Publication:Emerging Infectious Diseases
Geographic Code:1U9HI
Date:Aug 1, 2005
Words:4109
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